Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus

American Journal of Ophthalmology

Volumn 132, Issue 4, 2001, Pages 551-556

  Abu El Asrar, Ahmed M ^a,c   Desmet, Stefaan ^b   Meersschaert, Ann ^b   Dralands, Lieve ^b   Missotten, Luc ^b   Geboes, Karel ^b  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ADULT; AGED; ANGIOGENESIS; ARTICLE; CAROTID ARTERY OBSTRUCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; OCULAR ISCHEMIC SYNDROME; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINOPATHY;

ADULT; AGED; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC RETINOPATHY; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; RETINA; VIMENTIN;

EID: 0034810383     PISSN: 00029394     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9394(01)01127-8     Document Type: Article

References (43)

1. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J 1992;6:3051-3064.
2. Nathan C. Inducible nitric oxide synthase: what difference does it make? J Clin Invest 1997;100:2417-2423.
3. Nogawa S, Forster C, Zhang F, Magayama M, Ross ME, ladecola C. Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc Natl Acad Sci USA 1998;95:10966-10971.
4. Krupinski J, Vodovotz Y, Li C, et al. Inducible nitric oxide production and expression of transforming growth factor-beta 1 in serum and CSF after cerebral ischaemic stroke in man. Nitric Oxide 1998;2:442-453.
5. Zhang F, ladecola C. Temporal characteristics of the protective effect of aminoguanidine on cerebral ischemic damage. Brain Res 1998;802:104-110.
6. Gales E, Golanov EV, Feinstein DL, Kobylarz KA, Glickstein SB, Reis DJ. Cerebellar stimulation reduces inducible nitric oxide synthase expression and protects brain from ischemia. Am J Physiol 1998;274:H2035-H2045.
7. Niwa K, Takizawa S, Kawaguchi C, Kamiya U, Kuwahira I, Shinohara Y. Expression of inducible nitric oxide synthase immunoreactivity in rat brain following chronic hypoxia: effect of aminoguanidine. Neurosci Lett 1999;271:109-112.
8. Ziehe M, Morbidelli L, Masini E, et al. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 1994;94:2036-2044.
9. Murohara T, Asahara T, Silver M, et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 1998;101:2567-2578.
10. Ziche M, Morbidelli L, Choudhuri R, et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not fibroblast growth factor-induced angiogenesis. J Clin Invest 1997;99:2625-2634.
11. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda F, Ziehe M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol 1996;270:H411-H415.
12. Papapetropoulos A, García-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997;100:3131-3139.
13. Shizukuda Y, Tang S, Yokota R, Ware A. Vascular endothelial growth factor-induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase C δ activity. Circ Res 1999;85:247-256.
14. Jadeski LC, Lala PK. Nitric oxide synthase inhibition by N (G)-nitro-L-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am J Pathol 1999;155:1381-1390.
15. Buttery LD, Springall DR, Andrade SP, et al. Induction of nitric oxide synthase in the neo-vasculature of experimental tumours in mice. J Pathol 1993;171:311-319.
16. Jude EB, Boulton AJ, Ferguson MW, Appleton I. The role of nitric oxide synthase isoforms and arginase in the pathogenesis of diabetic foot ulcers: possible modulatory effects by transforming growth factor beta 1. Diabetologia 1999;42:748-757.
17. Sjoholm A. Aspects of the involvement of interleukin-1 and nitric oxide in the pathogenesis of insulin-dependent diabetes mellitus. Cell Death Differ 1998;5:461-468.
18. Rungger-Brandie E, Dosso AA, Leuenberger PM. Glial reactivity, on early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci 2000;41:1971-1980.
19. Barber AJ, Antonetti DA, Gardner TW, and The Penn State Retina Research Group. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. Invest Ophthalmol Vis Sci 2000;41:3561-3568.
20. Leith E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Diabetes 1998;47:815-820.
21. Bek T. Immunohistochemical characterization of retinal glial cell changes in areas of vascular occlusion secondary to diabetic retinopathy. Acta Ophthalmol Scand 1997;75:388-392.
22. Mizutani M, Gerhardinger C, Lorenzi M. Müller cell changes in human diabetic retinopathy. Diabetes 1998;47:445-449.
23. Goureau O, Hicks D, Courtois Y, De Kozak Y. Induction and regulation of nitric oxide synthase in retinal Müller glial cells. J Neurochem 1994;63:310-317.
24. Dighiero P, Reux I, Hauw JJ, Fillet AM, Courtois Y, Goureau O. Expression of inducible nitric oxide synthase in cytomegalovirus-infected glial cells of retinas from AIDS patients. Neurosci Lett 1994;166:31-34.
25. Koeberle PD, Ball AK. Nitric oxide synthase inhibition delays oxonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp Neurol 1999;158:336-381.
26. Hattenbach LO, Allers A, Klais C, Koch F, Hecker M. L-Arginine-nitric oxide pathway-related metabolites in the aqueous humor of diabetic patients. Invest Ophthalmol Vis Sci 2000;41:213-217.
27. Yilmaz G, Esser P, Kociek N, Aydin P, Heimann K. Elevated vitreous nitric oxide levels in patients with proliferative diabetic retinopathy. Am J Ophthalmol 2000;130:87-90.
28. ladecola C, Zhang F, Casey R, Nagayama M, Ross ME. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 1997;17:9157-9164.
29. Dawson VL, Brahmbhatt HP, Mong JA, Dawson TM. Expression of inducible nitric oxide synthase causes delayed neurotoxicity in primary mixed neuronal-glial cortical cultures. Neuropharmacology 1994;33:1425-H30.
30. Goureau O, Regnier-Richard F, Courtois Y. Requirement for nitric oxide in retinal neuronal cell death induced by activated Müller glial cells. J Neurochem 1999;72:2506-2515.
31. Oku H, Yamaguchi H, Sugiyama T, Kojima S, Ota M, Azuma I. Retinal toxicity of nitric oxide released by administration of a nitric oxide donor in albino rabbit. Invest Ophthalmol Vis Sci 1997;38:2540-2544.
32. Morgan J, Caprioli J, Koseki Y. Nitric oxide mediates excitotoxic and anoxic damage in rate retinal ganglion cells cocultured with astroglia. Arch Ophthalmol 1999;117:1524-1529.
33. Dawson VL, Dawson TM. Nitric oxide neurotoxicity. J Chem Neuroanat 1996;10:179-190.
34. Amin RH, Frank RN, Kennedy A, Eliott D, Puklin JE, Abrams GW. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 1997;38:36-47.
35. Montrucchio G, Lupia E, DeMartino A, et al. Nitric oxide mediates angiogenesis induced in vivo by platelet-activating factor and tumor necrosis factor-α. Am J Pathol 1997;151:557-563.
36. Papapetropoulos A, Desai KM, Rudic RD, et al. Nitric oxide synthase inhibitors attenuate transforming-growth-factor-beta 1-stimulated capillary organization in vitro. Am J Pathol 1997;150:1835-1844.
37. Misko TP, Moore WM, Kasten TP, et al. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur J Pharmacol 1993;233:119-125.
38. Neufeld AH, Sawada A, Becker B. Inhibition of nitric-oxide synthase 2 by aminoguanidine provides neuroprotection of retinal ganglion cells in a rat model of chronic glaucoma. Proc Natl Acad Sci USA 1999;96:9944-9948.
39. Wautier JL, Guillausseau PJ. Diabetes, advanced glycation end products and vascular disease. Vase Med 1998;3:131-137.
40. Hames HP, Strodter D, Weiss A, Bretzel RG, Federlin K, Brownlee M. Secondary intervention with aminoguanidine retards the progression of diabetic retinopathy in the rat model. Diabetologia 1995;38:656-660.
41. Tilton RG, Chang K, Hasan KS, et al. Prevention of diabetic vascular dysfunction by guanidines. Inhibition of nitric oxide synthase versus advanced glycation end-product formation. Diabetes 1993;42:221-232.
42. Nilsson BO. Biological effects of aminoguanidine: an update. Inflam Res 1999;48:509-515.
43. Freedman BI, Wuerth JP, Cartwright K, et al. Design and baseline characteristics for the Aminoguanidine Clinical Trial in overt Type 2 Diabetic Nephropathy (ACTION II). Control Clin Trials 1999;20:493-510.